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Expression of ezrin in subventricular zone neural stem cells and their progeny in adult and developing mice

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Abstract

Ezrin is a member of the ezrin–radixin–moesin (ERM) family of proteins, which link the cytoskeleton and cell membrane. ERM proteins are involved in pivotal cellular functions including cell–matrix recognition, cell–cell communication, and cell motility. Several recent studies have shown that ERM proteins are expressed in specific cell types of the adult rostral migratory stream (RMS). In this study, we found that ERM proteins are expressed highly in the early postnatal RMS and the ventricular zone of embryonic cerebral cortex, suggesting that these proteins may be expressed by neural progenitors. Furthermore, whereas ezrin previously was found to be expressed exclusively by astrocytes of the adult RMS, we found that ezrin-expressing cells also expressed the markers for indicating neuroblasts in vivo and in vitro, and that ezrin expression by neuroblasts decreases progressively as neuroblasts migrate. Using in vitro differentiation of adult neural stem cells, we found that ezrin is expressed by neural stem cells and their progeny (neuroblasts and astrocytes), but not by oligodendrocytic progeny. Collectively our findings demonstrate that adult neural stem cells and neuroblasts express ezrin and that ezrin may be involved in intracellular actin remodeling.

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Abbreviations

SVZ:

Subventricular zone

OB:

Olfactory bulb

RMS:

Rostral migratory stream

ERM:

Ezrin–radixin–moesin

CNS:

Central nervous system

VZ:

Ventricular zone

DG:

Dentate gyrus

References

  • Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–457

    Article  PubMed  CAS  Google Scholar 

  • Antoine-Bertrand J, Ghogha A, Luangrath V, Bedford FK, Lamarche-Vane N (2011) The activation of ezrin–radixin–moesin proteins is regulated by netrin-1 through Src kinase and RhoA/Rho kinase activities and mediates netrin-1-induced axon outgrowth. Mol Biol Cell 22:3734–3746

    Article  PubMed  CAS  Google Scholar 

  • Berryman M, Franck Z, Bretscher A (1993) Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J Cell Sci 105(Pt 4):1025–1043

    PubMed  CAS  Google Scholar 

  • Cleary MA, Uboha N, Picciotto MR, Beech RD (2006) Expression of ezrin in glial tubes in the adult subventricular zone and rostral migratory stream. Neuroscience 143:851–861

    Article  PubMed  CAS  Google Scholar 

  • Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci Off J Soc Neurosci 17:5046–5061

    CAS  Google Scholar 

  • Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716

    Article  PubMed  CAS  Google Scholar 

  • Fehon RG, McClatchey AI, Bretscher A (2010) Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11:276–287

    Article  PubMed  CAS  Google Scholar 

  • Fievet BT, Gautreau A, Roy C, Del Maestro L, Mangeat P, Louvard D, Arpin M (2004) Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J Cell Biol 164:653–659

    Article  PubMed  CAS  Google Scholar 

  • Gimeno L, Corradi A, Cobos I, Consalez GG, Martinez S (2004) Ezrin gene, coding for a membrane-cytoskeleton linker protein, is regionally expressed in the developing mouse neuroepithelium. Gene Expr Patterns 4:749–754

    Article  PubMed  CAS  Google Scholar 

  • Gronholm M, Teesalu T, Tyynela J, Piltti K, Bohling T, Wartiovaara K, Vaheri A, Carpen O (2005) Characterization of the NF2 protein merlin and the ERM protein ezrin in human, rat, and mouse central nervous system. Mol Cell Neurosci 28:683–693

    Article  PubMed  Google Scholar 

  • Haas MA, Vickers JC, Dickson TC (2007) Rho kinase activates ezrin–radixin–moesin (ERM) proteins and mediates their function in cortical neuron growth, morphology and motility in vitro. J Neurosci Res 85:34–46

    Article  PubMed  CAS  Google Scholar 

  • He M, Zhang ZH, Guan CB, Xia D, Yuan XB (2010) Leading tip drives soma translocation via forward F-actin flow during neuronal migration. J Neurosci 30:10885–10898

    Article  PubMed  CAS  Google Scholar 

  • Jayasundar JJ, Ju JH, He L, Liu D, Meilleur F, Zhao J, Callaway DJ, Bu Z (2012) Open conformation of ezrin bound to PIP2 and to F-actin revealed by neutron scattering. J Biol Chem 287:37119–37133

    Google Scholar 

  • Johnson MW, Miyata H, Vinters HV (2002) Ezrin and moesin expression within the developing human cerebrum and tuberous sclerosis-associated cortical tubers. Acta Neuropathol 104:188–196

    Article  PubMed  CAS  Google Scholar 

  • Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG (2006) Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 9:779–786

    Article  PubMed  CAS  Google Scholar 

  • Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148

    Article  PubMed  CAS  Google Scholar 

  • Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981

    Article  PubMed  CAS  Google Scholar 

  • Moon Y, Kim HJ, Kim JY, Kim H, Kim WR, Sun W (2011a) Different expression of human GFAP promoter-derived GFP in different subsets of astrocytes in the mouse brain. Anim Cells Syst 15:268–273

    Article  CAS  Google Scholar 

  • Moon Y, Kim JY, Choi SY, Kim K, Kim H, Sun W (2011b) Induction of ezrin-radixin-moesin molecules after cryogenic traumatic brain injury of the mouse cortex. NeuroReport 22:304–308

    Article  PubMed  CAS  Google Scholar 

  • Oudin MJ, Gajendra S, Williams G, Hobbs C, Lalli G, Doherty P (2011) Endocannabinoids regulate the migration of subventricular zone-derived neuroblasts in the postnatal brain. J Neurosci Off J Soc Neurosci 31:4000–4011

    Article  CAS  Google Scholar 

  • Persson A, Lindwall C, Curtis MA, Kuhn HG (2010) Expression of ezrin radixin moesin proteins in the adult subventricular zone and the rostral migratory stream. Neuroscience 167:312–322

    Article  PubMed  CAS  Google Scholar 

  • Schaar BT, McConnell SK (2005) Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci USA 102:13652–13657

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Kim H, Moon Y (2010) Control of neuronal migration through rostral migration stream in mice. Anat Cell Biol 43:269–279

    Article  PubMed  Google Scholar 

  • Takeuchi K, Kawashima A, Nagafuchi A, Tsukita S (1994) Structural diversity of band 4.1 superfamily members. J Cell Sci 107(Pt 7):1921–1928

    PubMed  CAS  Google Scholar 

  • Tsukita S, Oishi K, Sato N, Sagara J, Kawai A (1994) ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 126:391–401

    Article  PubMed  CAS  Google Scholar 

  • Tsukita S, Yonemura S (1999) Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J Biol Chem 274:34507–34510

    Article  PubMed  CAS  Google Scholar 

  • Turunen O, Wahlstrom T, Vaheri A (1994) Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J Cell Biol 126:1445–1453

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Kaneko N, Asai N, Enomoto A, Isotani-Sakakibara M, Kato T, Asai M, Murakumo Y, Ota H, Hikita T, Namba T, Kuroda K, Kaibuchi K, Ming GL, Song H, Sawamoto K, Takahashi M (2011) Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J Neurosci Off J Soc Neurosci 31:8109–8122

    Article  CAS  Google Scholar 

  • Wichterle H, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18:779–791

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Omelchenko T, Hall A (2010) LKB1 tumor suppressor protein regulates actin filament assembly through Rho and its exchange factor Dbl independently of kinase activity. BMC Cell Biol 11:77

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the Korean Ministry of Education, Science and Technology, via the Brain Research Center of the 21st century Frontier Program in Neuroscience (2012K001108) and the National Research Foundation of Korea (20120006433, 20120005815, 2012049933).

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Correspondence to Woong Sun.

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Moon, Y., Kim, J.Y., Choi, S.Y. et al. Expression of ezrin in subventricular zone neural stem cells and their progeny in adult and developing mice. Histochem Cell Biol 139, 403–413 (2013). https://doi.org/10.1007/s00418-012-1048-7

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  • DOI: https://doi.org/10.1007/s00418-012-1048-7

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